Little is known concerning the processing of innocuous thermoreceptive information in the CNS of the monkey. The aim of the present study was to confirm the prediction, based on recent studies in cat and monkey, that there must be a prominent spinothalamic (STT) projection of cooling-specific spinal cord lamina I neurons to the posterior part of the ventral medial nucleus (VMpo) of the monkey thalamus. 2. Experiments were performed on four cynomolgus monkeys anesthetized with pentobarbital sodium. A detailed mapping of somatosensory thalamus was performed in each animal, and VMpo was identified by recordings from clusters of thermoreceptive-specific and nociceptive-specific (NS) neurons. Stimulating electrodes were then implanted in VMpo. Tungsten microelectrodes were used to record the responses of neurons in the superficial dorsal horn of the lumbosacral spinal cord. 3. Many spontaneously active lamina I neurons were found that were inhibited by radiant warming and that responded to innocuous cooling of the hindpaw. These cooling-specific (COLD) neurons were excited by small temperature drops below skin temperature and increased their discharge with decreasing skin temperature. They were not excited by thermally neutral mechanical stimuli applied to the receptive fields. In passing, we also characterized with natural stimulation a few NS neurons reponsive to pinch and/ or noxious heat, multimodal (HPC) neurons responsive to noxious heat, pinch, and cold stimuli, and wide-dynamic-range neurons responsive to both innocuous and noxius cutaneous stimuli that were encountered in lamina I. 4. Twenty lamina I COLD cells were identified as STT neurons by antidromic activation from the contralateral VMpo. The mean conduction latency for these units was 26.1 ms, which corresponds to a mean conduction velocity of approximately 8.0 m/s. They were not antidromically activated from an electrode in the region of the ventral posterior nucleus in the thalamus. In addition, we antidromically activated from VMpo four NS units and three HPC cells. 5. These findings demonstrate for the first time the existence of a prominent direct projection of specific COLD lamina I STT cells to thalamus in the monkey. This is consistent with clinical inferences in humans and with prior results in cats. This result confirms that the dense lamina I STT projection to VMpo demonstrated in anatomic studies includes COLD cells, and it supports the role of VMpo as a thalamic relay nucleus for pain- and temperature-related information.
